Competition for epidermal area, instead of coordination, between stomata and vein patterns in Ficus (Moraceae) with different growth forms

Abstract

The coordination of stomatal conductance and hydraulic conductance in plants is often indicated by a positive relationship between stomatal density and vein density. However, when both hydraulic conductance and stomatal conductance increase simultaneously, there can be conflicting demands that causes a competition for epidermal space, leading to a negative association between stomatal density and vein density. Therefore, the interplay between these traits and how it is influenced by different growth forms is still a subject of debate. In this study, we conducted a common garden experiment to investigate the coordination between stomata, veins, and photosynthesis in 22 species of Ficus with varying growth forms, including free-standing, hemiepiphyte, and climber forms. Our findings revealed that growth form had a significant impact on stomatal and hydraulic traits in Ficus. Hemiepiphyte species exhibited a drought tolerance strategy during their epiphytic stage, characterized by thinner leaves with low stomatal density but higher stomatal size, as well as higher leaf water content and vein density (vein length per area, VLA) compared to free-standing and climber fig species. Climber figs, on the other hand, showed a lower specific leaf area and net photosynthetic rate compared to the other two forms. Contrary to many of previous studies, we found a negative correlation between VLA and stomatal density, as well as a positive correlation between VLA and stomatal size. Our study also suggests that other variables contribute to the variation in photosynthetic rate in Ficus, as stomatal morphology and vein density did not account for the observed variation significantly. Additionally, our analysis revealed non-random patterns of evolution for stomatal density, stomatal size, and VLA. The correlation between vein density and stomatal morphology was observed throughout the evolutionary history of Ficus, which appears to be associated with the diversification of growth forms. Overall, our findings support the “competition hypothesis,” which proposes antagonistic demands on the epidermal area between stomata and veins in Ficus.